J Korean Radiol Soc 1998; 39: 693-698

Solitary Nodular Bronchioloalveolar ofthe : 1 Prediction ofHistology at High-Resolution CT

Hyun-JungJang, M.D., Kyung Soo Lee, M.D., Yookyung Kirn, M.D. 2 Myung-HeeShin, M.D.3, In Wook Choo, M.D., SeungHoonKirn, M.D. WonJae Lee, M.D., Hong SikByun, M.D., SangJinKirn, M.D.4

Purpose : The purpose of this study is to describe the characteristic high-resol­ ution (HR) CT findings of solitary nodular bronchioloalveolar carcinoma (BAC) of the lung which are valuable for specific diagnosis ofthe disease. Materials and Methods : HRCT scans of 46 patients (31 with malignant and 15 with benign ) with a solitary pulmonary seen on were distributed in random order and analyzed retrospectively. Two blinded observers jointly analyzed the marginal and internal characteristics of nodules as seen on HRCT, and decisions on the findings were reached by consensus. Stepwise discriminant analysis for characteristic findings ofBAC was performed. Results : The most frequent CT findings ofBAC (n= 15) were internal bubble lu­ cency (1 4/15, 93 %)(p=O .-OOl), area of ground-glass opacity (12/1 5, 80 % ; average 58 % of tumor volume)(p=O.OOOl), pleural tag(12/15, 80 % ; p=0.097), and lobulated and spiculated margin(8/1 5, 53 % ; p=0.459). Findings of ground-glass opacity (p=O.OOOl) and bubble lucency (p=0.0187) appeared to be discriminant in the diagnosis of BAC. Conclusion : Peripheral pulmonary nodules containing an area of ground-glass opacity associated with internal bubble-lucency are characteristic ofBAC. Specific histologic diagnosis of solitary nodular BAC can be suggested by careful analysis ofHRCT findings.

Index words : Lung, CT Lung, nodule Lung , diagnosis Lung neoplasms, CT

Bronchioloalveolar carcinoma (BAC) of the lung is a type(7, 8). With its favorable prognosis and distinctive subtype of (1 - 4). Its unique features radiologic features, solitary nodular BAC, the most are its histologic lepidic growth pattern using the al­ commonly presenting form, is generally considered a veolar septa as a stroma and its mode of aerogenous separate clinical entity(5, 7, 9). Reported CT findings of spread(5 -7). BAC displays a broad spectrum ofradi이­ solitary nodular BAC include a peripheral subpleural ogic features that can be categorized as solitary nodu­ location, internal bubble lucency or pseudocavitation, lar, segmental or lobar, or the diffuse multinodular heterogeneous attenuation, irregular margins and pleural tag. These findings are not specific, however, 'Department of Radiology, Samsung Medical Center, College of Medicine, Sung they are frequently observed in adenocarcinoma and Ky un Kwan University 'Department of Diagnostic Radiology, College of Medicine, Ewha W omans Uni. large cell carcinoma ofthe lung(lO). versity In over 70 % of patients, nod ular BAC less than 3 cm JDepartment of Center for Health Promotion, Samsung Medical Center 'Department of Diagnostic Radiology, Yongdong Severance Hospital in diameter responds to (ll) and when less Received November 3, 1997; Accepted July 24, 1998 than 2cm, the reported five-year survival rate is 98. 2 Address reprint requests to : Kyung Soo Lee, M.D. , Department of Radiology %(3). Early recognition is therefore important. In a re­ Samsung Medical Center, # 50 Irwon.Dong, Ka ngnam-Ku Seoul 135.230, South Korea. Tel. 82. 2.3410.2511 Fax.82. 2.341O. 2559 cent study involving a small number of patients, we

- 693 Hy un-Jung Jang. et al : S이 itary Nodular 8ronchioloalveolar Carcinöma of the Lung reported that a localized area of ground-glass opacity, Image interpretation with internal bubble lucency on high-resolution CT The HRCT scans of all patients were randomly dis­ (HRCT), is an early finding of BAC(12). The result of 2- tributed and assessed by two experienced chest radiol­ [fluorine-181-fluoro-2-deoxy-D-glucose (FDG) positron ogists, whose decisions were consensual. Observers emission tomography(PET), however, may be nega­ had no knowledge of clinical or pathologic data other tive(12 - 14). In addition, presumably because of spar­ than the age and sex of the patients; they were not se cellularity, we have experienced false negative aware of which diseases were included in the study results of percutaneous needle aspiration of nor, the frequency ofindividual diseases. these . So as not to overlook this surgically The evaluated HRCT findings included the follow­ curable disease, solitary nodular BAC needs to be ings : (a) size (b) edge, classified as smooth, lobulated, recognized, if possible, on the basis of specific imaging spiculated, or lobulated and spiculated; the presence features. of (c) open sign, (d) positive bronchus sign, The aim of this stud y is to determine the findings (e) bubble lucency, (f) pleural tag, (g) satellite lesion, (h) which most effectively discriminate between solitary air-crescent sign, (i) ground-glass opacity and the per­ nodular BAC and other pulmonary nodules. Our ap­ centage of the nodule it accounted foι estimated visu­ proach involves the use of HRCT followed by stepwise ally; and (j) calcification and its characteristics, classi­ discriminant analysis. fied as central, laminated, popcorn-like, nodular, or stippled. Open bronchus sign (previous CT air bron­ chogram) was considered to be present if there was Materials and Methods patent branching airway structure(s) within a nodule Selection of patients and image acquisition (15, 16). Positive bronchus sign was regarded as pres­ This study involved 46 patients in whom solitary ent if a bronchus extended up to, and entered the nod­ pulmonary nodules were seen on chest radiographs, ule(17). Bubble lucency was considered to be present if and who underwent HRCT between November 1994 there were small scattered areas of air attenuation (oval and May 1997. Nodules were consecutively proved by or round) within a nodule(15). 'Pleural tag' was de­ surgery and satisfied the following inclusion criteria fined as linear structure(s) originating from the margin on chest radiographs: less than 3 cm in maximal dimen­ of a nodule and extending peripherally to contact the sion, a location peripheral to that of segmental bronchi, pleural surface. ‘Satellite nodule' was defined as one or and with no enlarged hilar or mediastinal lymph more micronodule(s) surrounding the dominant nod­ nodes. The patients were 20 men and 26 women, and ule. 'Air-crescent sign' was defined as curvilinear air were aged between 16 and 78 (mean, 58.8) years. All density around a nodule. underwent surgery and definite diagnoses were made on the basis of histopathologic examination of spec­ Statistical analysis imens. Pathologic entities included lung (n=30) Using the chi square test, the frequency of each CT ; BAC(n = 15), adenocarcinoma(n = 11), squamous cell finding of BAC was compared with that of other carcinoma(n=2), large cell carcinoma(n=l), and muc­ nodules. A p-value less than 0.05 was considered sig­ oepidermoid carcinoma(n=1), and benign nodules(n= nificant. 16); (n=7), (n=5), and tub­ Age, sex, and CT features were evaluated using step­ erculoma(n =4) wise discriminant analysis; this identifies the discrim­ For CT examinations, a GE HiSpeed Advantage scan­ inant CT findings that most accurately measure the ner (General Electrical Medical Systems, Milwaukee, characteristics of solitary nodular BAC 뻐 d permit dif­ WI, U.S.A) was used. Before obtaining conventional ferentiation between various cell types of CT images using the helical technique (lO-mm and benign nodules. The objective is to maximize sep­ collimation, pitch of one) with administration of con­ aration of groups by weighting and combining the trast(lOOmL of Iopamiro 300: IopamidoL Bracco, Mil­ discriminant variables in some linear form. A user-sel­ an, Italy), thin-section (1-mm collimation) CT scans of ected criterion is applied, and the single best discrimi­ all patients were obtained at 3-mm (n=19) or 5-mm nating variable is selected. All remaining potential var­ (n=27) intervals throughout the nodule. Scan data iables are then tested(18, 19). In this study, the ability were reconstructed using a bone algorithm(HRCT). to classify cases correctly using the discriminant func­ Images were obtained both at mediastinal (WW: 400, tion was measured using Fischer’s exact test. The mag WL: 30) and lung window (WW: 1500H, WL: -700) nitude of the coefficient in the resulting discriminant settings. function reflects the unit of measurement as well as its

- 694 J Korean Radiol Soc 1998; 39 : 693-698 relative contribution. SAS software (system for Win­ 05. Calcification was stippled. dows version 6.11) was used Stepwise discriminant analysis showed that areas of ground-glass opacity (p=O.OOOl) and bubble lucency (p=0.0058) individually were useful for distinguishing Results BAC from other cell types of lung cancer and benign Solitary nodular BAC was found in seven men and lesions(Table 2). eight women, aged between 39 and 72 (mean, 59) years The BAC ranged in size from 1. 5 to 3.0 (mean, 2.4)cm. Discussion The most frequent CT findings of BAC were internal bubble lucency (14/1 5, 93 %) (p=O.OOI) (Figs. 1 and 2), Kuhlman et al (10) reviewed the thin-section CT area of ground-glass opacity (1 2/15, 80 %, [average 58 (2 - 5 mm collimation) findings of solitary nod ular BAC % of tumor volume]) (p=O.OOOI) (Figs. 1-3), pleur­ in 30 patients. In their series, peripheral or subpleural altag (12/15, 80 %) (p=0.097) (Figs. 1 and 3), and lob­ location(25/30, 83 %), irregular margins forming a star ulated and spiculated margin (8 /1 5, 53 %) (p=0.459) pattern(22/30, 73 %), pleural tag(70 %), pseudocavita­ (Figs. 1 and 3) (Table 1). Open bronchus sign, positive tion(18/30, 60 %), and heterogeneous attenuation (17 / bronchus sign, calcification, and satellite nodule were 30, 57 %) were suggested CT criteria for solitary nodu­ seen in four(27 %), three(20 %), one(7 %), and one (7 %) lar BAC. In their study, however, there is considerable patient, respectively ; all p values were greater than O. overlap of CT findings of BAC, particularly between

Fig. 1. Bronchioloalveolar carcinoma in a 63-year-old woman. High-resol­ ution CT scan obtained at level of azygos arch shows area of ground­ glass opacity showing internal bub­ ble lucencies (arrows) and open bron­ chus sign (arrowhead) in right upper lobe. Pleural tag is seen. Fig. 2. Bronchioloalveolar carcinoma in a 60-year-old woman. Lung win­ dow of high-resolution CT scan obtained at level of great vessels shows localized area of ground-glass opacity in right upper lobe. AIso note internal bubble lucency(arrow).

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Table 1. CT Findings of 46 Nodules with Various Histology Histology ofPulmonary Nodules

CTFindings BAC Adeno S qu따no Large Mucoepi Tuberc Hamar Asper (n=15) (n = ll) (n=2) (n=l) (n=l) (n=4) (n=5) (n=7) Internal bubble lucency* 14(93)+ 2 (18) 1 ( 50) 0 1 (100) 3 (75) 0 3 (42) Area of ground-glass opacity* 12 (80) 2 (18) 0 0 0 1 (25) 0 4(58) average % oftumor volume 58 15 0 0 0 20 0 13 Pleural tag 12 (80) 9 (82) 1 ( 50) 0 0 3 (75) 0 4(58) Lobulated & Spiculated margin 8 (53) 5 (46) 2 (100) 0 1 (100) 2 (50) 0 2 (29) Open bronchus sign 4 (27) o ( 0) 0 0 1 (100) o ( 0) 0 2 (29) Positive bronchus sign 3 (20) 3 (27) 1 ( 50) 0 0 0 0 0 Calcification 1 ( 7) 2 (18) 0 0 1 (100) 1 (25) 2(4이 2 (29) Satellite nodule 1 ( 7) 1 ( 9) 0 0 1 (100) 3 (75) 0 5 (71) Air crescent sign 0 0 0 0 0 0 0 5 (71) * statistically significant in BAC compared to frequency of other nod ules, + numbers in parenthesis are percentage, BAC: bronchioloalveolar carcinoma, Adeno : adenocarcinoma, Squamo: squamous cell carcinoma, Large : large cell carcinoma, mucoepi : mucoepidermoid carcinoma, Tuberc : tuberculoma, Hamar: hamartoma, Asper : aspergilloma

Table 2. CT Factors Ranked by Stepwise Discriminant Anal­ addition, their study used a thicker (2 - 5 mm collima­ ysis in Ability to Enable Differentiation ofBronchioloalveol­ tion) CT section than ours(I.0-mm collimation). Groun­ ar Carcinoma from Other Histologic Types of Pulmonary d-g1ass opacity could not, therefore, be appropriate1y Nodules assessed in their study, and there might be differences Factors Partial R2 F Statistics probability in the assessment of edge characteristics as well as nod­ Area of ground-glass 0.4631 37.790 0.0001 u1e size. opacity In our previous study invo1ving a small number of Bubble lucency 0.1638 8.424 0.0058 cases, we concluded that a focal area of ground-g1ass Age 0.1254 6.022 0.0184 opacity, seen on HRCT, is “ one of a variety of appear­ ances of BAC"(12). The present study demonstrated R2: a measure ofthe goodness offit ofthe model. F: a value of the distribution of the model divided by that of that areas of ground-g1ass opacity within a nodu1e is error the most va1uab1e finding for discriminating BAC from other pu1monary nodu1es, is a common and generally adenocarcinoma and large cell undifferentiated carci applicable finding(80 %). noma. In our study, the most frequent CT findings of Our results can be exp1ained on the basis of current BAC were internal bubble lucency or pseudocavita­ patho1ogic concepts for adenocarcinoma( 2 - 4, 20) tion(93 %), area of ground-glass opacity (80 %) with an Most are believed to deve10p either average of 58 % of tumor vo1ume, p1eural tag(80 %), de novo or through the stage of atypica1 adenomatous and lobulated and spicu1ated margin(53 %). In stepwise hyperp1asia (bronchioloa1veo1ar adenoma [BAA])(2, 4, discriminant ana1ysis, areas of ground-g1ass opacity 21). The latter concept ofmultistep carcinogenesis and appeared to be the most discriminant finding, followed progression has been described by Miller et a1. as an by bubble 1ucency, for distinguishing BAC from other adenoma-carcinoma sequence, which is well known in histo1ogic types ofpulmonary nodules. the co1on(20). Bronchio1oa1veolar carcinoma with re­ With regard to the prevalence of characteristic fin­ placement growth pattern is often accompanied by dings of BAC, our resu1ts were somewhat different BAA at the periphery and may consist of hetero from those of Kuhlman et a1( 1O). However, there is a geneous components showing different stages of dif­ significant difference in scan technique that may be ferentiation that strong1y supports the 1atter way of de­ partly responsib1e for the different prevalence. They ve1opment. In contrast, nonreplacement-type aden­ used a variety of window widths and 1evels which ocarcinoma, which shows a pattern of largely solid and ranged from 1, 164 to 1,800 and from - 180 to - 500, destructive growth, is thought- because ofthe absence respectively; we, on the other hand, used a standard of such stepwise progression - to be de novo type(2). It window width of 1,500 and window 1evel of - 700. In has been well documented that BAA appears as a small - 696 J Korean Radiol Soc 1998; 39: 693-698 nodule with ground-glass opacity(22). Our previous Kurokawa et al (3) and 74.2 % (175/236) according to study revealed that nonmucinous nodular BAC, in Noguchi et al.(2). Those studies showed that BAC which pathologic findings showed that the tumor accounted for a considerable proportion of small re­ grows as a single celllayer along alveolar walls, can also sectable adenocarcinomas. manifest as a focal area of ground-glass opacity(12). In a Because we included only nodules confirmed by study by Noguchi et al(2), BACs were grouped into surgery, there might be selection bias in interpreting three distinctive structural patterns: type A, with the CT appearances of benign nodules. In fact, except minimal thickening of alveolar septa; type B, with a for symptomatic aspergillomas with typical CT feat­ similar appearance to type A but with fibrotic foci due ures of air crescent sign, the appearance of all benign to alve이ar c이 lapse; type C, with foci of fibroblastic nodules in this study was somewhat malignant or pr이 iferation which appeared to be an advanced stage equivocal. Conversely, because we included cases of of types A and B. For these two types the prognosis is surgically confirmed benign nodules of malignant ap­ excellent, with a five-year survival rate of 100 %. For pearance, the discriminant findings suggested by our type C, on the other hand, the rate is 74.8 %, which is study may in clinical practice be more helpful in similar to the average for overall small adenocarcin­ distinguishing nodules according to their histologic omas. In the light of those studies, we can speculate differences. that areas of ground-glass opacity within the nodule is In conclusion, among many reported features of soli­ the most representative feature of BAC to ref1ect its tary nodular BAC seen on HRCT, an area of ground­ developing nature. glass opacity appears to be the most discriminant find­ We found that among non-BAC , adenocar­ ing for distinguishing BAC from other histologic types cinoma occasionally simulated the findings of BAC, of pulmonary nodules, followed by bubble lucency. with-in two of eleven patients-areas of ground-glass Being familiar with these discriminative findings in opacity and bubble lucency(Fig. 4). The pathology of combination with other characteristic findings dis­ those two cases was 'adenocarcinoma with BAC cussed, we can strongly suggest a specific histologic di­ features'. It is therefore more plausible to regard this agnosis of solitary nodular BAC. This unique lung can­ similar appearance as a ref1ection ofmicroscopic (BAC) cer with favorable prognosis cannot, therefore, be features, as seen on HRCT, than to consider those missed even when the results of percutaneous needle findings as nonspecific for BAC. Though there is no aspiration biopsy are negative. pathologic explanation, our experience has shown that simple pulmonary eosinophilia can totally mimic such characteristic features of BAC when it occurs as a soli References tary lesion. Because ofits transient and f1eeting nature, 1. Kreyberg L. Hist%gica/ typing of /ung tumors. Voll. Inter­ follow-up CT scans obtained within six to eight national histological classification of tumors, Geneva, 1967, weeks-if these indicate the disappearance of focal area Wold Health Organization. of ground-glass opacity-can solve the problem(23). 2. Noguchi M, Morikawa A, Kawasaki M, et al. Small adenocar­ In comparison to other studies of equal or greater cinoma of the lung. Histologic characteristics and prognosis. sample size(lO, 15), the proportion of BAC relative to Cancer 1995 ; 75: 2844-2852 3 ‘ Kurokawa T, Matsuno Y, Noguchi M, Mizuno S, Shimosato Y adenocarcinoma was much higher (15 versus 11) in this Surgically curable “ early" adenocarcinoma in the periphery of study. Although the incidence of BAC varies widely, the lung. Am J Surg Patho/ 1994; 18: 431-438 from three percent of all pulmonary in a 4. Clayton F. The spectrum and significance of bronchioloalveolar Baltimore series to 38 percent in a Japanese series(4), It carcinomas. Patho/ Annu 1988 ; 23: 361-394 is thought to be partly due to differences in study de­ 5‘ Epstein DM. Bronchioloalve이 ar carcinoma. Semin Roentgeno/ 1977; 12: 207-214 sign. In the study of Zwirewich et al.(15), the mean di­ 6. Edward cw. Alveolar carcinoma: a review. Thorax 1984; 39 ameter of adenocarcinoma and that of BAC are 3.5cm 166-174 and 3.1 cm, respectively. On the other hand, our study 7. Hill CA. Bronchioloalveolar carcinoma: a review. Radi%gy was strictly limited to solitary pulmonary nodules con­ 1984; 150: 15-20 secutively proved by surg 8. Adler B, Padley S, Miller RR, Mííller NL. High-Resolution CT of bronchioloalveolar carcinoma AJR 1992; 159 : 275-277 9. Miller WT, Husted J, Firman D, Atkinson B, Pietra G Bronchioloalveolar carcinoma: two clinical entities with one pathologic diagnosis. AJR 1978 ; 130: 905-912 10. Kuhlman JE, Fishman EK, Kuhajda FP, et al. Solitary bronchiol­ oalveolar carcinoma: CT criteria. Radi%gy 1988 ; 167: 379-382

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II ‘ Greco RJ, Steiner RM , Goldman S, Cotler H, Patchefsky A, 17. Swensen SJ. Focal lung disease: CT and high-resolution CT

Cohn HE. Bronchioloalveolar cell carcinoma of the lung‘ Ann applications. RadioGmphics 1994; 14: 169-181 Thorac Surg 1986; 41: 652-656 18. Armitage P. Statistica/ methods in medical research. 3rd ed 12. Jang HJ, Lee KS, Kwon OJ, Rhee CH, Shim YM, Han J Oxford: Blackwell, 1974; 302-344 Bronchioloalveolar Carcinoma: focal area of ground-glass at­ 19. Kleinbaum DE, Kupper LL. Applied regression an띠)잉 s and other tenuation at thin-section CT as an early sign. Radiology 1996; mu/tivariate methods. North Scituate, Mass: Duxbury, 1978; 199 : 485-488 41 4-446 13. Kim BT, Lee KS, Kim Y, et al. Solitary nodular bronchioloal­ 20. Miller RR, Nelems B, Evans KG , Mtiller NL, Ostrow DN veolar carcinoma of the lung: FDG PET findings. AJR (in press) Glandular neoplasia of the lung. A proposed analogy to colonic 14. Scott WJ, Schwabe JL, Gupta NC, Dewan NA, Reeb SD, Sug­ tumors. Cancer 1988 ;61: 1009-1014 imoto JT. Positron emission tomography of lung tumors and 21. Shimosato Y, Noguchi M, Matsuno Y. Adenocarcinoma of the mediastinal Iymph nodes using [18F] . Ann lung: its development and malignant progression. Lung Cancer Thorac Surg 1994; 58 : 698-703 1993; 9: 99-108 15. Zwirewich CV, Vedal S, Miller RR, Müller NL. Solitary pul­ 22. Kushihashi T, Munechika H, Ri K, et al. Bronchioloalveolar ad­ monary nodule: high-resolution CT and radiologic-pathologic enoma of the lung: CT-pathologic correlation. Radiology 1994; correlation. Radiology 1991 ; 179: 469-476 193: 789-793 16. Kuriyama K, Tateishi R, Doi 0 , et al. Prevalence of air 23. Kim Y, Lee KS , Choi D-C, Primack SL, 1m J-G. The spectrum of

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대한밤사선의학회지 1998; 39 : 693-698

단일폐결절성 세기관지폐포암 : 고해상전산화단충촬영상의 조직학적 예단 1

1 성균관대학교 의과대학 방사선과학교실 2 이화대학교 의과대학 방사선과학교실 3 성균관대학교 의과대학 예방의학교실 4 연세대학교 의과대학 방사선과학교실

장현정 · 이경수 · 검유경 2 • 신명희 3 • 주인욱 · 김승훈 · 이원재 · 변홍식 · 김상진 4

목 적 : 단일폐결절성 세기관지 폐포암에서 조직학적으로 진단을 예 측할 수 있는 특징적인 고해성 전산화단 층촬영 (HRCT) 소견을기술하고자하였다. 대상 및 방법 : 단순흉부촬영상 단일폐결절을 가진 46 명의 환자를 무작위로 배열하여 HRCT 소견을 후향적으 로분석하였다 .31 명은 악성， 15명은 양성 결절을가지고 있었다. 병리진단을모른 채 두명의 방사선과의사가합 의로 폐결절의 경계 빛 내부 소견을 분석하였으며 세기관지 폐포암의 특정적 소견을 알기 위해 다단계 식별분석 을시도하였다. 결 과 · 기관지 폐포암 (n=15) 의 가장 흔한 소견은 내부 기포형 저음영(1 4/15 ， 93%) (P=O.OOl), 간유리형 병변(1 2/15 ， 80%, 종괴의 58 % 용척) (P=O.OOl), 늑막꼬리(1 2/ 15 ， 80%) (P=0.097) 및 엽성 및 침상 경계 (8/15 ， 53%) 였다. 간유리형 병변 (P=O.O O1)과 내부 기포형 저음영 (P = 0.0187) 은 세기관지 폐포암의 진단에 있 어 가장 식별 능력이 있는소견이었다. 결 론 : 내부에 기포형 저음영을 가진 간유리형 병변을 포함하는 원위부 폐결 절은 세기관지 폐 포암의 특징적 소견이다. 그러므로 HRCT 소견을 세멸하게 분석하면 단일폐 결절성 세기관지 폐포암을 특이적으로 진단할 수 있다.

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